Primate-like mammals:

A stunning diversity in
the tree tops

It is in the early Paleocene that we first encounter animals
in the fossil record which show strong links to our own order,
the primates. Surprisingly, early primate-like forms are best
known from continents that are today, apart from their
southernmost corners, not inhabited by primates other than human
beings: Europe and North America. This unusual geographical
occurrence can be explained by the warm, even subtropical
conditions that existed far into the north during Paleocene time.
Favorable conditions also allowed other exotic animals like
crocodiles to thrive at high latitudes. Yet the importance and
diversity of primate-like mammals in the Paleocene faunas of
Europe and North America is remarkable.

During the Paleocene most primate-like animals belonged to a
group called Plesiadapiformes. Traditionally, the plesiadapiforms
have been regarded as archaic members of the order Primates.
Although plesiadapiforms are similar to modern primates in a
number of characteristics of their skeleton, they were still on a
much lower evolutionary level, comparable perhaps to the living
tree-shrews (1). Modern primates are unique
among mammals in their adaptation to life in the trees. Their
capabilities of grasping and leaping allow rapid locomotion in
this environment, which is in turn related to the large brain
size they have developed. As far as we know, plesiadapiforms also
spent most of their time in the trees. However, they lack
adaptations for fast leaping as we see them in modern primates
and were not capable of moving as quickly through the trees. In
addition, their brain was still very small in comparison to
modern primates. On the other hand, plesiadapiforms soon acquired
traits that are unusual for later primates, especially enlarged
incisors that are superficially similar to those of rodents. This
suggests that the plesiadapiforms were not the direct ancestors
of modern primates, but rather a branch that split off from the
mainline of primate evolution (from today's point of view) at an
early date. The picture is complicated by other still existing
orders of mammals that must be close to primates on the
evolutionary tree: The tree-shrews (order Scandentia), the
colugos or "flying lemurs" (order Dermoptera), and
perhaps the bats (order Chiroptera), although the latter are only
distantly related according to recent molecular studies (2, 3). Where plesiadapiforms
fit in between all of these is still hotly debated (4). However, many scientists are today reluctant
to call these archaic forms primates and regard them instead as
members of a separate order Plesiadapiformes (5).

Figure 1: Hypothetical restoration of the Early
Paleocene Purgatorius,
one of the earliest known primate-like mammals. From (28).

The most primitive known plesiadapiform, and one of the
earliest, is the famous Purgatorius, an animal comparable
to a small rat in size (6). Only the remains
of the teeth and jaws are known for Purgatorius. Their
structure is not far from the pattern that we would expect in the
common ancestor of all placental mammals, presumably a small
generalized insectivore. Yet the teeth of Purgatorius show
some traits that are characteristic of both plesiadapiforms and
true primates. Their design suggests an animal that fed not only
on insects but also on some kind of soft plant material, probably
fruits. Restorations often show Purgatorius scurrying
under the feet of Late Cretaceous dinosaurs like Tyrannosaurus
and Triceratops. Actually one species, Purgatorius
ceratops, was named with this picture in mind. However,
nearly all fossils of Purgatorius are from the Early
Paleocene of North America. Only a single tooth has ever been
found together with the remains of dinosaurs, and this tooth
could be a contamination from Paleocene rock that was mixed by
mistake with Cretaceous material when the collectors sieved the
sediments. Even if no mixing happened during collecting, it is
possible that something similar occurred nearly 65 million years
ago: The deposits producing the single Purgatorius tooth
were probably laid down during early Paleocene time by a river
cutting deeply into Cretaceous sediments, mixing the fresh
remains of Paleocene mammals with older fossils such as dinosaur
teeth (7). Although unknown primate-like
animals may have existed before the end of the Mesozoic, we still
have no convincing evidence of them.

If we want to
know more about early primate-like beings than jaws and teeth can
tell us, we have to take a look at later, more specialized forms.
The best known plesiadapiforms are the Plesiadapidae, one of the
most successful families of Paleocene mammals (1,
8). Plesiadapids were chipmunk- to
marmot-sized animals that had a superficially rodent-like
dentition, with a pair of robust, enlarged incisors that is
followed by a long gap without teeth (diastema) in later forms.
Whereas the lower incisors are relatively simply built and form a
kind of scoop together, the upper ones are more complicated, with
three separate cusps in front and another one behind, a
configuration that has been compared to mittens. Unlike the
enlarged incisors of rodents, the front teeth of plesiadapids
neither have a self-sharpening cutting edge nor are they
ever-growing, so they were probably utilized for one or several
purposes different from gnawing. In advanced plesiadapids the
cheek teeth are becoming flattened and the enamel is increasingly
crenulated, which suggests that these animals mainly subsisted on
a vegetable diet, perhaps on leafs and some fruits.

Figure 2: Skull of Plesiadapis
tricuspidens from the Late Paleocene of
France, vaguely resembling that of a rodent with its enlarged
incisors and the long diastema in front of the cheek teeth. Note
that the orbits of plesiadapiforms are not yet completely
enclosed by bone, unlike those of true primates. From (8).

Skull and skeleton of plesiadapids are most
completely known in the late Paleocene Plesiadapis. This
genus probably arose in North America and colonized Europe on a
landbridge via Greenland. Thanks to the abundance of the genus
and to its rapid evolution, species of Plesiadapis play an
important role in the zonation of Late Paleocene continental
sediments and in the correlation of faunas on both sides of the
Atlantic. Two remarkable skeletons of Plesiadapis, one of
them nearly complete, have been found in lake deposits at Menat,
France (8, 9, 10). Although the preservation of the hard parts
is poor, these skeletons still show remains of skin and hair as a
carbonaceous film - something unique among Paleocene mammals.
Details of the bones are better preserved in fossils from Cernay,
also in France, where Plesiadapis is one of the most
common mammals. The rodent-like skull of Plesiadapis is
relatively broad and flat, with a long snout and orbits still
directed to the side, unlike the forward facing eyes of modern
primates that enable three-dimensional vision (1,
6, 11). Although its
braincase was small according to today's standards, it was larger
than in the contemporary hoofed mammals,
for instance. Plesiadapis had mobile limbs that terminated
in strongly curved claws, and it sported a long bushy tail which
is beautifully preserved in the Menat skeletons. The way of life
of Plesiadapis has been much debated in the past. Climbing
habits could be expected in a relative of the primates, but
tree-dwelling animals are rarely found in such high numbers.
Based on this and other evidence, some paleontologists have
concluded that these animals were mainly living on the ground,
like today's marmots and ground squirrels (8, 10). However, more recent investigations have
confirmed that the skeleton of Plesiadapis is that of an
adept climber, which can be best compared to tree squirrels or to
tree-dwelling marsupials such as possums (1, 6).

Figure 3: Restoration of the widespread genus Plesiadapis,
showing the clawed hand and feet and the bushy tail. From (29).

It is noteworthy that early researchers surmised a close
relationship between plesiadapids and the bizarre aye-aye of
Madagascar, the only living primate with a rodent-like dentition.
Later students have rejected such evolutionary ties, and the
aye-aye is now regarded as a member of the same primate stock as
lemurs and loris (12). Yet the aye-aye may be
ecologically similar to a rare genus of plesiadapids, the
squirrel-sized Chiromyoides from the Late Paleocene of
Europe and North America (1, 6).
Chiromyoides can be characterized as a super-robust
version of Plesiadapis, with considerably shortened and
deepened jaw and muzzle, and with extremely robust incisors that
bear sharp cutting edges. Obviously its feeding mechanism had to
withstand much higher forces than in other plesiadapids. Jaws and
teeth of Chiromyoides closely resemble those of the
aye-aye, which was sometimes called Chiromys in previous
times - hence the name of the plesiadapid. The aye-aye uses its
enlarged incisors to gnaw into wood in search of grubs. Chiromyoides
may have occupied a similar niche in the forests of the Late
Paleocene. This specialization would also explain its rarity in
the mammal communities of that time. It may be of interest to
note that a second group of Early Tertiary mammals, the Apatemyidae, evolved very
similar adaptations, probably even approximating the aye-aye more
closely than Chiromyoides.

A second family of plesiadapiforms, the
Carpolestidae, is characteristic of Paleocene faunas in North
America, although it never becomes as dominant as the
plesiadapids (1, 6, 13, 14). Like the latter,
carpolestids have enlarged incisors, the lower ones simply built
and the upper ones mitten-shaped. However, they are much smaller,
ranging from the size of a mouse to that of a rat. Carpolestids
have developed their last lower premolars into enormous blades
with serrated cutting edges, a condition termed plagiaulacoid
that evolved independently in several groups of mammals, most
prominently in the archaic multituberculates.
In carpolestids these saw-like teeth worked against the also
enlarged but flattened and rasplike third and fourth premolar of
the upper jaw. This mechanism was probably used to process
vegetable diet with a high content of fibers such as fruits, nuts
or succulent shoots, a diet perhaps supplemented by some insects.
The evolution of this highly specialized adaptive complex can be
tracked in the successive North American genera Elphidotarsius,
Carpodaptes and Carpolestes that form the mainline
of carpolestid evolution in North America. The mouse-sized Elphidotarsius
from the Middle Paleocene of North America is still very similar
to primitive plesiadapids, but its last lower premolar already
foreshadows the blade-like form of advanced carpolestids. By Late
Paleocene time, the diagnostic traits of the family are well
established in Carpodaptes, and they are further refined
in Latest Paleocene species of Carpolestes ("fruit
stealer"), the last of the North American carpolestids.

Figure 4: Skull of the Late Paleocene Carpodaptes.
The saw-like premolar in the lower jaw characterizes the
Carpolestidae. From (30).

Carpolestids have long been known from little more than teeth
and jaws, but a recently discovered nearly complete skeleton of Carpolestes
simpsoni now sheds more light on their appearance and biology
(15, 16). Carpolestes
simpsoni was a small creature with a body weight of only 100
g, and obviously it was highly adapted to life in the trees. Its
big toe could be opposed to the other toes, enabling the animal
to firmly grasp smaller branches with its feet just like it could
with its hands. The big toe of Carpolestes simpsoni
carried a nail, something that allowed to develop far better
tactile abilities than if the tip of the toe was covered by a
claw. Nails were previously only known in true primates. Their
presence in a plesiadapiform documents emphatically how these
archaic forms were adapting to their arboreal environment,
sometimes in ways also pursued by later primates. Unlike the
first true primates, however, Carpolestes shows no
adaptations for leaping.

Another family of highly
specialized plesiadapiforms are the Picrodontidae, tiny animals
such as the type genus Picrodus that occur with only a few
species in the Middle and Late Paleocene of North America (1, 6). Picrodontids have long
knifelike lower incisors, similar to those of other
plesiadapiforms, but their cheek teeth are highly modified. The
first upper and lower molars are extremely enlarged, and all
molars form wide, shallow basins with heavily wrinkled enamel.
Emphasis was clearly on increasing surface area in order to mash
some kind of soft food. More abrasive food would have obliterated
the low crowns of the teeth even during the very short life span
that is typical of such small mammals. The specialized molars are
so similar to those of certain recent bats that early researchers
even considered picrodontids as possible members of that order,
otherwise first known from the Early Eocene (17).
Today this resemblance is regarded as convergent, but it provides
important clues about the feeding habits of picrodontids. Like
those bats, picrodontids probably fed on nectar and pollen, a
highly nutritious diet that is very easy on the teeth, and
perhaps also on tree sap and juicy fruit. A skull fragment of the
picrodontid Zanycteris displays a relatively narrow
muzzle. Any other adaptation of picrodontids to their particular
ecological niche remains open to speculation.

Even smaller plesiadapiforms
belong to the Micromomyidae (1, 6,
18). The family includes diminutive forms from
the Late Paleocene to Early Eocene of the Rocky Mountain region
which carry such appropriate names as Micromomys and Tinimomys
(the suffix -mys meaning "mouse"). These animals
may just have weighed about 30 g - distinctly less than the
smallest living primate, the mouse-lemur Microcebus of
Madagascar. An amazingly complete skeleton of a still unnamed
micromomyid has recently been discovered in Latest Paleocene
sediments. It suggests a tiny creature of only 20 g body weight
that was highly adapted for climbing and may have been able to
suspend itself from trees (15). Mammals of
such small body weight are typically insectivorous, and in fact
the sharp teeth of Micromomys confirm that this was a
committed insect hunter.

Other plesiadapiforms seem to have
harvested the diverse fruits of the widespread tropical to
subtropical forests. Members of the Paromomyidae are
characterized by molars that are squared off and flattened,
forming large basins that would have been well suited for mashing
fruit. Tree sap and insects may have complemented this diet (1, 6, 15, 19). The dental trends of paromomyids can be
traced back to Paromomys from the Middle Paleocene of
North America. In advanced forms such as Ignacius and Phenacolemur
the central incisors become extremely enlarged and slender, and a
large diastema develops behind them, like in plesiadapids. Both Ignacius
and Phenacolemur were long-lived genera that range from
the Late Paleocene to the Middle Eocene. Thus they were among the
last surviving plesiadapiforms - living fossils in a world that
was since long inhabited by true primates.

Figure 6: Skull of Ignacius
graybullianus from the Latest Paleocene to
Early Eocene of North America (stippled parts reconstructed).
Note general resemblance of the dentition to Plesiadapis
(Figure 2) but even longer incisors in the lower jaw. Scale bar 1
cm. From (11).

Paromomyids play an important role in a hypothesis from the
1990s which assumes close relationships between the
plesiadapiforms and the colugos or "flying lemurs". The
latter form one of the smallest existing orders of mammals, the
Dermoptera, with just two species from Southeast Asia (1). Colugos have a gliding membrane that runs
from behind their ears to the tip of their tail and that allows
them to glide over large distances. The gliding membrane of
colugos even extends between the digits of hand and foot, which
enables them to control flight better than other gliding mammals.
Because of similar hand structures in dermopterans and
paromomyids, it has been claimed that the latter also possessed a
gliding membrane. This and other evidence has led some
researchers to the conclusion that plesiadapiforms are ancient
dermopterans, today's colugos being the relics of a once diverse
order of mammals that forms the sister group of primates (19, 20, 21).
More complete fossils, however, do not confirm the idea that
paromomyids were gliders. Instead paromomyids appear to have been
squirrel-like creatures that could scamper both in the trees and
on the ground (15, 22).

Even if no special relationships
may exist between plesiadapiforms and colugos, other Paleocene
mammals may prove to be early dermopterans. Among these are the
plagiomenids, an enigmatic group that first appears in the Middle
Paleocene of North America (1, 23).
Plagiomenids are rare in most faunas, but they can dominate at
individual localities, which may indicate particular habitat
requirements. Fossils of the Latest Paleocene plagiomenid Planetetherium,
for example, occur in abundance at a coal mine in Montana but are
hardly known elsewhere. The animals must have found ideal
conditions in the heavy forested or swampy environment
represented by the mine deposits (24, 25). Interestingly, during Eocene times some
plagiomenids even thrived on Ellesmere Island, the northernmost
part of Canada that lies well within the Arctic Circle. Although
climatic conditions where then of course much warmer than today,
the animals living there must still have faced the winter
darkness of such high latitudes (at least 76° North at that
time) (1).

Figure 7: Hypothetical restoration of the Latest
Paleocene Planetetherium
as a glider similar to today's colugos or "flying
lemurs". From (28).

The supposed link between plagiomenids and colugos is
exclusively based on similarities of their dentitions, which have
long been the only plagiomenid fossils. The lower incisors of
plagiomenids, for instance, consist of two lobes, perhaps an
early stage in the evolution towards the specialized comblike
lower incisors that today's colugos use for grooming.
Similarities of the cheek teeth, though somewhat vague, also
suggest that plagiomenids may be early dermopterans. If this is
the case, it would not be surprising to find gliding adaptations
in Paleocene plagiomenids, given the fact that other mammals had
evolved into full-fledged bats by the Early Eocene. This idea
cannot be directly tested today with the available fossils. The
link between plagiomenids and colugos has been weakened, however,
by a recently discovered skull of the Latest Paleocene to Early
Eocene Plagiomene, which shows some important anatomical
differences in comparison to dermopterans (23).
In face of this conflicting evidence, complete plagiomenid
skeletons are urgently needed to solve the mystery of these
intriguing animals.

Plesiadapiforms, and perhaps
plagiomenids, belong to a first wave of primate-like mammals that
flourished in the Paleocene. These archaic forms were replaced in
the Eocene by true primates, which are called euprimates in
technical jargon. The earliest known euprimates belong to the
families Adapidae and Omomyidae (4). Both
groups already possessed the advanced grasping and leaping
adaptations and the correlated large brain that characterize
modern primates. The adapids were similar and perhaps related to
the lemurs of Madagascar and to the loris of tropical Africa and
Asia. They mainly include larger animals that were presumably
active during the day. Typical omomyids were small creatures with
large eyes that suggest activity during the night. Omomyids may
include the ancestors of the Southeast Asian tarsiers, nocturnal
hunters of small prey that are great leapers and habitually cling
to branches in a vertical position. Adapids and omomyids appear
all of a sudden in the fossil record of Europe and North America
at the beginning of the Eocene, which suggests they immigrated at
that time from another part of the world, either from Africa or
from Asia. Supposed euprimates have in fact been described from
the Paleocene of these continents. Petrolemur and Decoredon
from the Paleocene of China have been advanced as early members
of the Adapidae and Omomyidae respectively. Both are poorly
known, however, and it is not even sure that these animals are
related to the primates at all (26). A more
promising candidate was Altiatlasius from the Late
Paleocene of Marocco, one of the few mammals that are known from
the Paleocene of Africa. Originally described as an omomyid, Altiatlasius
seemed to support the role of Africa as the center of primate
evolution. Yet a recent study came to the result that Altiatlasius
is no euprimate but belongs to a mainly European group of
plesiadapiforms which dispersed into Africa across the ancient
Tethys seaway (5, 27).

We thus still lack conclusive evidence about the early history
of true primates - a history which began without question during
Paleocene times, if not earlier (4).
Nevertheless, we have ample evidence of the extraordinary success
which their relatives, the plesiadapiforms, experienced in early
Cenozoic faunas. As we have seen, the teeth of plesiadapiforms
document a variety of feeding strategies, ranging from
insectivores to generalized vegetarians and specialized pollen-
and nectar-feeders, and we are just beginning to appreciate other
aspects of their biology like locomotion. Hopefully, new
discoveries will one day fill in the gap that separates these
archaic forms from true members of our own order, the Primates.